Teaching the process of science with primary literature: Using the CREATE pedagogy in ecological courses

Abstract There have been numerous calls for improved pedagogical practices in biological education, and there is a clear need for such improvements in ecology and related curricula. Most ecology‐related texts lack pedagogy and are designed to be content‐rich. National initiatives, such as Vision & Change, provide guidance on undergraduate biology education, including increasing use of evidence‐based active learning, and taking a more conceptual and science practice skills approach. Biology education research is rich with evidence‐based teaching practices, which reveal that active learning approaches implemented in thoughtful ways lead to strong learning gains relative to lecture‐based course delivery. CREATE (Consider, Read, Elucidate the hypothesis, Analyze and interpret data, Think of the next Experiment) integrates evidence‐based active pedagogical practices into one approach to STEM education that focuses heavily on the process of science and science practice skills rather than content delivery by replacing the textbook with selected journal articles. The approach focuses on deep reading and analysis of primary literature; immersing students in the literature is an advantage of the pedagogy. CREATE was developed and tested in other biological disciplines (genetics and molecular biology) that have long been at the forefront of pedagogical best practices in biology. We transformed two upper‐level undergraduate ecological courses (Conservation Biology, and Biodiversity and Ecology) into CREATE courses. We provide examples of assignments, student work, and assessments of the approach, illustrating the various ways CREATE can be successfully implemented. The approach can be adopted in part, to ease into it and test it out, or in whole. We recommend that ecology teachers consider making their courses more active, if they have not already done so; adopting pedagogical practices embedded within CREATE can be a way to achieve active learning. The CREATE approach and other evidence‐based pedagogical best practices lead to strong learning gains and more inclusive learning environments.


Guide to reading the scientific literature in a CREATE course
In the CREATE strategy, you will never see an entire article until you have first read chunks of it. Generally, although not always, you will first download the introduction from Moodle, then the Methods and Results, and then the Discussion. You will be asked to resist the urge to find the article, either online or at the library. Reading the abstract or skipping ahead to the conclusions will detract from the learning experience that has been developed as the CREATE strategy. Here, I give you some generic advice to reading scientific literature.
First, effective readers take notes-it improves recall and comprehension. You may think you'll remember everything you read in researching class assignments, professional papers, proposals, or your thesis, but details slip away. Different sections of scientific papers will be read for several distinct purposes in this course, and thus your note-taking may vary from section to section. For instance, in the introduction you will focus on identifying concepts, linking them together, and integrating them with concepts or terms you learned previously. You may construct a concept map to bring to class, or you and your partners will construct one in class. In this way, you will build your ecological knowledge. In Methods sections, you will focus on translating the written description of experimental design into a sketch, or cartoon.

You will first have access to the introduction
As you read the introduction, write down every word that you don't understand. You're going to have to look many of them up, although you can discern many meanings contextually and it will become easier as you build your ecological knowledge. It will be important to keep in mind that you won't understand the paper if you don't understand the vocabulary. Scientific words have precise meanings, as you know by now.
In addition, keep notes on other terms and concepts that you do know. Ultimately, for each introduction, you will build a concept map, linking together known and new concepts and terms. Some terms will be important and fundamental concepts, others will describe methods, processes, taxonomic groups, or environmental factors. In addition to identifying concepts and understanding terms, you will be challenged to read the introduction closely to discern the relationships between these terms. This will allow you to more easily develop a concept map for the introduction and determine the big question of the paper. You should be able to understand why this research has been done in order to explain it to your peers in class.

Identify the specific question(s)
This part may come up in the introduction, or we may get to it after the methods and results are read; it just depends on the structure of the paper and the flow I have developed for the class. For this, try to determine what fundamental ecological question(s) the authors are trying to address with their research. There may be multiple questions or just one. Write them down as part of your note-taking. If it's the kind of research that tests one or more null hypotheses, identify it/them.

Now read the methods section. Draw a diagram for each experiment, showing exactly what the authors did.
What did the researchers do? The CREATE strategy uses cartooning of methods, where you will take the described methods and sketch a picture that represents what the researchers did. We will then compare cartoons to be sure that there is consensus on what was done, how the experiment was designed, what the controls and sample sizes were, etc. Include as much detail as you need to fully understand the methods and experimental design. You don't need to understand complex analytical methods (such as stable isotope analysis or multivariate statistics), but you should understand what the method was used for and what it is supposed to show. While you won't need to know the methods in enough detail to replicate the experiment, you're not ready to move on to the results until you can explain the basics of the methods to someone else.

Read the results section
Annotation is used to identify components in the figures and tables and to highlight your main points right on the figure or table from the original research. Use the text of the results to help identify the main points. Don't try at this stage to determine what the results mean, just write down the results and point them out in the figures and tables. There may be some challenges at this point if statistical tests are employed that you don't understand. This is one place, among several others, where I will provide some remediation and guidance.

Interpretation occurs before you read the discussion
Using the hypotheses, questions, cartoons, diagrams, and charts and/or graphs, determine what the results mean. Link your interpretations to your concept maps, both current and previous. Analyze your interpretations in light of the experimental methods and goals of the researchers. After all figures and tables have been analyzed, revise your concept map for the paper.

Read the discussion section
Restate what the authors think their results mean. Do your interpretations agree with them? Can you or your peers come up with alternative ways of interpreting the results? Do the authors identify any weaknesses in their own study? Do you see any that the authors missed? What do they propose to do as a next step? Propose your own next steps or next experiments.

Now, go back to the beginning and read the abstract
Does it match what the authors said in the paper? Does it fit with your interpretation of the paper?

A couple of key points to keep in mind
For adequate understanding of an article, you should be prepared to read a section two, three, or even up to four times. You will often be amazed to discover that what seemed completely incomprehensible on the first reading appears to make perfect sense on subsequent readings. You should be comforted to know that even experienced scientists must read articles over and over again. Furthermore, there will be things you simply do not understand because 1) you do not have the adequate background, 2) they are just too complicated, or 3) they simply do not make sense. Do not overlook this last possibility simply because you see something in print.
You should be prepared to do some work in order to acquire sufficient background for adequate understanding of an article. This will include: 1) looking up definitions of words you do not know; 2) looking up points made in references cited by the paper; 3) asking questions of people who may know, including your instructor!

Sketching methods (cartooning) and annotating results
Two key steps in the C.R.E.A.T.E. model (Consider Read, Elucidate the hypotheses, Analyze and interpret the data, and Think of the next Experiment) are cartooning and annotation, two approaches that will deepen your understanding of the primary literature and the connections between methods, results, and conclusions. This deeper understanding will also increase your understanding of ecological concepts.
Because of inexperience with ecological research methods, even if you read the methods sections you may not understand how studies or experiments are carried out. It is often difficult for undergraduates to visualize what goes on in a research study when reading a methods section. You will be asked to challenge yourself to read the methods closely and to visualize the experimental design on paper.
You will be asked to make sketches to represent what goes on in the laboratory or in the field in order to generate the data in particular figures. For many papers we will consider only a subset of the figures and tables so you will visualize the methods only for those results. It could be as simple as an annotated version of a figure that shows the experimental design of a study, as in the figure shown to the right. Annotations for this sketch might include sample sizes, response variables measured (which may actually require an additional cartoon), or species used.
Students often do not like the idea of "cartooning" initially, but it actually provides students with a completely different way to process the information you are reading. Your level of understanding will increase and your frustration will decrease because you have a different outlet to express the ideas presented to you. This is in contrast to reading and rereading and hoping you come to understand it. Cartooning encourages you to more fully understand the techniques and the rationale behind the experiments, the findings, and discover possible shortcomings. Consider this simple example to the right where a cartoon has been made from the directions to baking a cake and how varying any of the factors might lead to alterations in the outcome.
In order to draw something, you have to commit to a belief about what you are representing. That is, students who can bluff their way through a class discussion or successfully rearrange words from a methods section into a flowchart without actually understanding what the words mean are initially stymied when asked to visually represent the methods. Committing to a sketch means committing to an understanding of something not provided with the paper itself. As you figure out what to draw, you will find yourself going beyond a superficial interaction with the verbiage and begin to develop visualization skills. You will also develop metacognition ability as you define what you do and do not know about the methods. If you realize you can't represent a particular analysis in a sketch because you don't really understand it, then you know you need to look it up or ask your professor.
In class you will work with your groups to create a consensus cartoon or we will work as a class on the board. We must all be in agreement about what was done before we can proceed to determine what the results were and how they should be interpreted.
After cartooning is completed, you will annotate the figures or tables associated with each experiment or study (see below for an example). To do this, rewrite key information from the caption or narrative directly on the figure. This allows you to define what particular arrows are pointing at or what a highlighted box is highlighting or what the axes are or what the treatments or cases represent. In addition, you might have to identify the populations, label of histograms or best-fit curves, what was measured or what is represented in the data.
The information needed to identify figure components is present either in captions or in associated narratives. The tracking down of the descriptions of figures and tables helps you build careful reading skills and move beyond cursory skimming of papers. We will sometimes do this in class but you will also be asked to complete this before class so that we have time to discuss and interpret what you have annotated.
The final step in annotation, and the reading of the methods and results, is to retitle the figure and to determine what question or hypothesis was being addressed by the study. This involves paraphrasing the official figure title in your own words. In addition, defining the hypothesis being tested or question being asked helps you see the overall paper in the larger context of the science of ecology.
When you analyze the methods and results on your own, without having access to the conclusions, you will be encouraged to think independently about what conclusions you draw rather than to summarize outcomes as stated by the authors.
The next document is the 2018 syllabus for CP's Ecology course (8 pages). The last half contains the schedule of readings and activities. The readings are all coded by module and paper number. After the syllabus, the papers are decoded and full citations are provided for these papers.
A few notes: 1. The papers used are not static -they change over time, as new, better papers are discovered.
ing organisms in the context of their environment. We will explore major concepts and societal concerns in ecology, using case studies, the primary literature, observations, experiments, and the core competencies of science (data analysis, critical thinking, Ecology is an interdisciplinary science that examines interactions between organisms and their environment, and the relationship between evolution and these interactions. The interdisciplinary character of ecology allows us to understand nature by plac-effective communication, quantitative reasoning, and an understanding of the link between science and society).

Course description
Learning outcomes Big Picture Learning Outcome: By the end of this course, you should be able to apply ecological theory and concepts and the core competencies of science (data analysis, critical thinking, quantitative reasoning, and effective communication) to explain, relate, evaluate, and hypothesize about ecological phenomena. There is no ecology textbook in this course. We will read research papers from the primary literature that will allow us to launch into a deeper investigation of ecological terms, concepts, and data. knowledge. They include concepts, enclosed in circles or boxes, with relationships indicated by a connecting line linking concepts. Words on the line, referred to as linking phrases, specify the relationship.

 Cartoons of methods:
Cartooning is a way of representing the methods. Your challenge is to sketch the methods so that they accurately reflect what the researchers did.   Defining of questions or hypotheses: Summarizing the main questions, in your own words, is a powerful way to show that you understand the funda-Ecology Portfolio: You will create a portfolio in which you will keep assigned readings and accompanying assignments (detailed below). This portfolio will be collected 2 times during the semester and evaluated based on the quality and quantity of thought and effort. I will also check recent work and give you feedback, often in class.
The materials in your portfolio should be created by you alone , even if you worked with others during in-class exercises or in a study group outside of class. Directly copying portfolio materials from another student is a violation of the Honor Code. Your portfolio should reflect your own thoughts, style, and effort. Bring this to class with you every day.
You will create some or all of the following for each paper that we read:  Concept maps: Concept maps are graphical tools for organizing and representing mental questions or hypotheses.
 Analysis and interpretation of results: Determine the logic of each experiment, examine the correspondence between experimental design and results, interpret the significance of the data, and evaluate and criticize the authors' interpretations.
 Listing of key points: Make a list of the key points from the study, which can be drawn from the hypotheses, the annotations of figures and tables, and interpretation of results.
 Defining/describing the next experiment: The final challenge is to think creatively about what you would do next if you were the researcher.
Integrative Essays: Several written assignments will be used to assess your ability to integrate course material and concepts. These will be 2-3 page essays on topics related to papers we read and discuss in class, with the addition of other primary literature you research, analyze, and integrate.

Assignments, discussion, participation BIO 321: Ecology
The distribution and abundance of organisms

Communication and technology
Course announcements, reminders, and ecologyin-the-news messages will be conveyed via email and/or Moodle. This course uses Moodle for assignments and readings. Please be responsible in your use of paper and printing. I encourage you to read assignments electronically whenever possible; but bring your notes or devices to class! In the field, studying stream insect diversity, Fall 2001

Writing assignments
Population growth dynamics

A food web
You will find it convenient and helpful to meet with your peers to discuss assignments and readings. Keep in mind that your written work must be your own and should reflect your own understanding of the assignment. Perhaps a good approach to take is to read the assignment on your own, then discuss it with teammates, and then complete the assignment on your own. The assignments will be steps toward the content that you are building for your book. Often, I will expect you to show up with the work, and in other situations I'll ask you to produce something during class. Most of these items will eventually be incorporated in your book.
There will be three exams, one of which may be an oral exam. Dates are shown in the semester schedule. I will provide you with additional details and examples ahead of time. The first exam will be written, the second one will be an oral exam, and the final exam will be written.
We will frequently have small group and class discussions on the readings. I will call on volunteers or select non-volunteers to summarize the material, relate it to the material we are currently covering, relate it to the themes of the course, or answer any number of other questions. Your preparation for class on these days will count for class participation. In addition, we will often have short discussions regarding the textbook reading; this will encourage you to read ahead.
Be prepared for class, whether the format for that day will be group work, discussion, field trip, or laboratory exercise. Material covered in lecture will supplement the text, and understanding the lecture will depend upon your reading before class. Unavoidable absences may occur, and in such cases, will require a legitimate excuse. There will be many out-of-class assignments, the completion of which will be critical to your participation in class. If you don't do the assigned out-of -work class, you will not be able to effectively participate in class.

Assignments, discussion, participation, cont 'd BIO 321: Ecology
The distribution and abundance of organisms Tardiness is not acceptable. I start on time, and I expect you to be in class or at a meeting place when I begin; I will not wait for anyone for field trips. It's distracting and disrespectful to come in late. If you are going to be absent or late and think you have a valid excuse, see or e-mail me. This applies to assignments; any assignment not turned in on time, and without a valid excuse, will receive an automatic 10% deduction, with another 10% for each additional day it is late. Consistent absences, tardiness, non-participation, and unpreparedness will affect your participation/ attendance grade. You will not be graded on attendance per se, but I will always be taking notes on class participation and the quality of your in-and out-ofclass work. In short, if you are not present, you will not receive credit for participation or the miscellaneous homework/in-class assignments, and the quality of your personal portfolio will suffer.
There will be three short laboratory reports, written individually but based on group field/lab work. We will form groups using an online assessment tool called CATME -I will provide further instructions via e-mail. See manual for more information.

Attendance
Daily assignments Exams Three-spotted damselfish, Pomacentrus tripunctatus Class Lab assignments An example of a simple food web I am committed to accommodating students with learning or physical disabilities. Your success in this class is important to me. If there are circumstances that may affect your performance in this class, please let me know as soon as possible so that we can work together to develop strategies for adapting assignments to meet both your needs and the course requirements.
Davidson College values the diversity of its community and is an equal access institution that admits otherwise qualified applicants without regard to disability. The college will review requests for accommodations related to disability and will grant those that are determined to be reasonable and maintain the integrity of a program or curriculum. To make such a request or to begin a conversation about a possible request, please contact the Office of Academic Access and Disability Resources, which is located in the Center for Teaching and  The Math & Science Center (MSC) offers free assistance to students in all areas of math and science, with a focus on the introductory courses. Trained and qualified peers hold one-onone and small-group tutoring sessions on a drop-in basis or by appointment, as well as recap sessions ahead of reviews. Emphasis is placed on thinking critically, understanding concepts, making connections, and communicating effectively. In addition, students can start or join a study group and use the MSC as a group or individual study space. Located in the Center for Teaching & Learning (CTL) on the 1st floor of the Library, drop-in hours are usually Sunday through Thursday, 8-11 PM, but I will announce the schedule as soon as it comes out. Appointments are available. For more info, visit http://www3.davidson.edu/cms/x39569.xml.
The Speaking Center @ Davidson College offers the services of trained student tutors to support speaking across the curriculum. At any point of the process, from selecting a topic to delivering the speech, the Center can assist you in learning to speak, and speaking to learn. No appointment is necessary. Located in Chambers B39 (north basement), the Speaking Center includes private rooms, a camera and playback equipment, and resources to help students collaborate with tutors. Students wishing to keep copies of their presentations can bring recordable DVDs. The Writing Center is located near Studio D and the Center for Teaching and Learning in the Library. Hours for the Speaking and Writing Centers will be announced in class.

BIO 321: Ecology
The distribution and abundance of organisms

ASSIGNMENTS, PARTICIPATION & EVALUATION
Evaluation: The laboratory portion of your grade will be based on a total of 250 points to be distributed as follows; 1) one individual report on forest succession (70 points), 2) one individual report on ecological big data (90 points), 3) one individual report on pond community ecology (90 points), and 4) participation and attendance (included in overall P&A).

Results and Discussion
Our experiment showed that CO 2 concentration significantly changed FA concentration and composition in the diatom T. pseudonana used for copepod diet. The relative amount of PUFAs was significantly lower (t 4.48, p 0.004) and the amount of SFAs higher (t 3.37, p 0.015) at high pCO 2 compared to the low pCO 2 treatment ( Figure 1A). Essential PUFA concentrations were significantly reduced at high pCO 2 (Table S1) A separate experiment confirmed that the shift in FA occurred rapidly in response to changing pCO 2 in the diatom T. pseudonana. When transferred from high to low CO 2 , FA composition was already significantly different from its initial composition after 15 h ( Figure 1B) and FA components changed in the same direction as observed at constant high and low pCO 2 treatments. Similarly, a rapid transition in FA composition can be expected when algae are transferred from low to high pCO 2 , which was, however, not tested in our experiment. Though, a rapid reversible FA response to changing pCO 2 concentration has been reported in green algae [26]. The higher unsaturation levels of FAs in algae cells cultured at low pCO 2 compared to cells at high pCO 2 has been suggested to be partially a consequence of repressed FA synthesis, which promotes the desaturation of pre existing SFAs [26]. Recently it has been proposed that pH might act as a regulation signal for the formation of cell membranes, which are mainly composed of fatty acids, by controlling the production of its synthesizing enzymes [28]. A high environmental pCO 2 (low pH) can decrease the internal cell pH [29]. Therefore the increased amount of SFAs could be a mechanism to control the internal cell pH, as a membrane built of short chain FAs is less fluid and permeable to CO 2 . However, the cellular processes involved in FA synthesis under changing pH or pCO 2 levels are not fully understood.
Similar to FA modification in algal food, FA concentration and composition of adult copepods varied significantly between CO 2 treatments. The mean 6SD total amount of FAs in A. tonsa was significantly different across treatments (F (3, 8) 5.15, p 0.028) and higher when raised and fed with algae cultured at low pCO 2 , with 8.965.6 ng ind. 1 compared to 0.860.2 ng ind. 1 when both copepods and algal diet were cultured at high pCO 2 and to 2.360.5 ng ind. 1 in the crossed treatment combinations (Table  S1). Copepods raised and fed with algae at low pCO 2 contained high proportions of PUFAs relative to total FAs that are in the same range with reports in marine calanoids [30]. The PUFA fraction in copepods decreased from more than 30% at low pCO 2 to less than 5% at high pCO 2 (F (3,8) 54.51, p,0.001) (Figure 2A). The long chain highly unsaturated FAs DHA and ARA EPA, which are important components for growth and reproduction of consumers [31], decreased from 15% in copepods raised at low pCO 2 below detection limit in those at high pCO 2 (Table S1). Similarly, the proportion of MUFAs (monounsaturated fatty acids) varied significantly across treatments (F (3,8) 8.2, p 0.008) and decreased from around 20% at low pCO 2 to less than 10% at high pCO 2 . On the other hand, the relative amount of SFAs tripled in copepods at high pCO 2 ( Figure 2A) and FA compositions were different between treatments (F (3,8) 26.22, p ,0.001).
Contrary to our expectation, FA composition in copepods differed between individuals raised at low and high seawater pCO 2 , irrespective of the CO 2 level of their algal diet (Figure 2A). Because consumers are unable to synthesize PUFAs we expected that copepod FA composition in the crossed pCO 2 treatments of copepod culture and food algae (P L /Z H , P H /Z L ) would reflect changes in FA of their diet. Principal component analysis (PCA) of individual FAs in diet algae and copepods also showed distinctive clustering of the copepod groups raised at low and high pCO 2 treatments, irrespective of the CO 2 conditions of their diet algal culture ( Figure 2B), which was mainly explained by PUFAs and SFAs ( Figure S2). A GLM model supported that CO 2 concentra tion of the seawater used to raise copepods significantly negatively affected the relative proportion of PUFAs (p,0.001) and positively affected the proportion of SFAs in copepods (p,0.001), which was These findings suggests that the FA composition of algae changed rapidly when transferred from low pCO 2 culture media to high pCO 2 seawater used to raise copepods and vice versa. Since consumers are unable to synthesize PUFAs [30] and previous experiments showed that copepod growth is rather insensitive to CO 2 levels within OA predictions [19], [20], direct CO 2 effects on copepod FA synthesis seem unlikely. In our experiment, water and food was exchanged every second day and algae were in their exponential growth. Thus, we rather expect that high turnover rates and the ability of T. pseudonana to rapidly change the FA composition in a variable pCO 2 environment ( Figure 1B) are responsible for an adjustment in FA composition in the crossed treatments within the first day. Rapid modification in algae FA and the fact that A. tonsa has no lipid reserves [32] likely explains the absence of the influence from the algae culture media pCO 2 on copepod FA composition within both crossed treatment combi nations.
The CO 2 dependent dietary shift in FAs had a significant effect on A. tonsa growth and development. Copepods of the same age (10 d) showed a delay in stage development of 1 to 2 days at high pCO 2 ( Figure 2C). Egg production decreased from a median of 34 eggs female 1 d 1 at low water and food pCO 2 to less than 12 eggs female 1 d 1 in all other treatments, with the lowest production (5 eggs female 1 d 1 ) at high water and food pCO 2 ( Figure 2D). The egg production rate was significantly related to the ratio of PUFA:SFA and the content of DHA and ARA EPA within the female copepods (Table 1), consistent with other observations in zooplankton [33]. Copepod egg production raised at low pCO 2 and fed with algae grown at high pCO 2 produced significantly less eggs compared to copepods in the low pCO 2 treatment combination ( Figure 2D). This significant decline is most likely a result of the overall lower copepod FA quantity when fed with algae cultured at high CO 2 compared to food at low CO 2 (Table S1). Given that adult A. tonsa females invest the majority of their lipids into reproduction [34], the significant decrease of essential PUFAs due to low quality food algae is most likely the reason for PCA scores 1 explained 40% of the variability (see x axis of c) and was highly negatively correlated with 22:6n 3 (r 2 = 0.73), 20:4n 6+20:5n 3 (r 2 = 0.85), 18:3n 6 (r 2 = 0.73) and 16:1 (r 2 = 0.79), and positively with 22:1n 9 (r 2 = 0.25) and 18:1n 9t (r 2 = 0.57). PCA score 2 explained 17% of the overall variability (see y axis of c) and was strongest positively correlated with 24:0 (r 2 = 0.84). Loadings of the PC scores are shown in Figure S2). C) Stage distribution of A. tonsa individuals at day 10. C4, C5, C6 = copepodite stage 4, 5, and adult, respectively. D) Egg production rate (EPR) of incubated females (n = 12 per treatment level). EPR was significantly different between treatments (F (3, 44) = 18.02, p,0.001). Different letters above bars represent significant differences from a Tukey HSD test. The bars represent the 25 th , 50 th and 75 th percentiles, whiskers stand for the 10 th and the 90 th percentiles and black points show outliers. Legend refers to treatment combinations of copepod zooplankton (Z) and phytoplankton food source (P) at low (L) and high (H) pCO 2 . doi:10.1371/journal.pone.0034737.g002 Ocean Acidification Constrains Trophic Transfer PLoS ONE | www.plosone.org Table 51. Results of t-tests for the pre-and post-course Eco/Evo MAPS assessment based on whether students had taken AP Bio (A) and one-way ANOVAs based on their class year (B). In header rows, numbers in parentheses equal sample sizes, and in the